Paralytic strabismus is an ocular motility disorder occurring as a result of disease affecting one or more of the three cranial nerves which supply the extra-ocular muscles.1 Its occurrence in childhood may be due to congenital or acquired conditions and it may be a feature of a generalized disease or an isolated event.2,3
In a hospital-based review of 121 children, Harley1 found sixth nerve palsy to be the most common type of paralytic strabismus while in a population-based study Holmes2 found fourth nerve palsy to be the most prevalent in children. In a review of only acquired pediatric cranial nerve palsies, Kodsi and Younge4 noted that sixth nerve palsies were the most common.
About 30% of Harley’s patients had congenital cranial nerve palsies compared to 44% in Holmes’ study.1,2 The most common cause of acquired pediatric paralytic strabismus has been found to be trauma.1,2,4
Other causes include neoplasms, infections, and vas-cular and inflammatory conditions.1,2,4–6
Virtually all previous reports have emanated from studies on mainly Caucasian populations in North America and Europe.1,2,4–12 Much less is known about the distribution and etiology of paralytic strabismus in children of other ethnic groups, and in particular, data from Africa is lacking. Availability of such infor-mation would aid ophthalmologists in the differential diagnosis of paralytic strabismus in an African setting.
The aim of this study was therefore to review the profile of paralytic strabismus in children who pre-sented to a South African tertiary pediatric eye clinic over a 15-year period.
MATERIALS AND METHODS
The study was a retrospective, descriptive case series in which the records of all patients younger than 14 years diagnosed with paralytic strabismus at the Red Cross
Received 22 November 2011; revised 07 March 2012; accepted 02 May 2012
Correspondence: Bolutife Olusanya, Eye Clinic, Red Cross War Memorial Children’s Hospital, University of Cape Town, Cape Town, South Africa. E-mail: [email protected]; [email protected]
Paralytic Strabismus in South African Black and Mixed Race Children – A 15-year Clinic-based Review
Bolutife Olusanya, Christopher Tinley, and Rhian Grotte
Eye Clinic, Red Cross War Memorial Children’s Hospital, University of Cape Town, Cape Town, South Africa
ABSTRACT
Purpose: To describe the demographics and clinical profile of paralytic strabismus in South African black and mixed race children seen at a tertiary pediatric eye clinic.
Methods: A retrospective, descriptive case series of patients younger than 14 years diagnosed with paralytic strabismus at the Red Cross War Memorial Children’s Hospital in Cape Town, between 1996 and 2010.
Results: A total of 166 children were studied. Of these, 74% were of mixed race descent while 26% were black. The most commonly affected cranial nerve was the fourth (52%). The sixth nerve was involved in 39% of cases, while 5% and 4% had third nerve palsy and multiple cranial palsies, respectively. The majority of mixed race children (58%) had fourth cranial nerve palsies, while 54% of black children had sixth nerve palsies. The most common cause of paralytic strabismus was congenital (55%), followed by trauma (18%).
Conclusion: In this clinic-based study, paralytic strabismus was more common in mixed race children. Fourth nerve palsies predominated in mixed race children, whereas the majority of black children had sixth nerve palsies. Further population-based research is necessary to identify the determinants of ocular cranial nerve palsy in African children.
War Memorial Children’s Hospital between 1996 and 2010 were reviewed. Patients with myasthenia, ocular muscle disease and strabismus syndromes such as Duane syndrome, Brown syndrome, and congenital fibrosis of extraocular muscles were excluded. Also excluded were patients with restriction of ocular movements due to orbital wall fractures and orbital inflammatory processes. Ethical approval was obtained from the University of Cape Town Institutional Review Board and the research followed the tenets of the Declaration of Helsinki.
The Red Cross War Memorial Children’s Hospital in Cape Town is a large, government-administered, tertiary referral pediatric centre which treats children aged less than 14 years. The age limit of 14 years is a hospital criterion; therefore, children over that age are not treated nor admitted. The hospital serves the populations from the Western Cape (4.5 million people) as well as the Northern (0.8 million) and Eastern Cape Provinces (6.4 million). These three provinces account for 26% of the population of South Africa.13 The ethnic distributions in the Western and Northern Capes are similar and comprise approximately 50% mixed race, 30% black and 20% Caucasian, while in the Eastern Cape the black ethnic group predominates (85%).13 The overwhelming majority of patients seen at our hospital are of mixed race or black ethnicity. Caucasian children and children from other ethnic backgrounds invariably have health insurance and receive health care from pri-vate pediatricians and ophthalmologists.
The mixed race group is heterogeneous, with two distinct origins. The first, or “colored,” community is made up of descendants of early intermarriages between European settlers and black natives. The Cape Malays, on the other hand, have historical and genetic ties with ancestors from South-East Asia. The black population has gradually migrated to the Western Cape and belongs mainly to the Xhosa-speaking tribe.
All patients with paralytic strabismus had been referred by local primary healthcare providers, general practitioners or hospital pediatricians and were all evaluated by a consultant pediatric ophthalmologist at our clinic. During evaluation, each child underwent a comprehensive medical history and ocular and orthop-tic examination. The children also had comprehensive evaluations by a pediatric neurologist and/or neuro-surgeon. When indicated based on clinical findings, neuro-imaging with computerized tomography and/or magnetic resonance imaging was performed to confirm or exclude intracranial pathology.
For the purpose of this study, the etiology of para-lytic strabismus was classified as congenital, traumatic, neoplastic, infection, aneurismal, or undetermined. Congenital cranial nerve palsy was defined as the onset of paralytic strabismus at birth or in the first few months of life, in the absence of post-natal etiology; or onset of an abnormal head posture before the age of 6 months, based on history obtained from caregivers. Traumatic cranial nerve palsy was defined as the onset of paralytic
strabismus soon after head trauma, with or without loss of consciousness. Neoplastic cranial nerve palsy was defined as paralytic strabismus associated with intracranial neoplasm, including those occurring as a complication of surgical excision. Post-infective cranial nerve palsy was defined as onset of paralytic strabismus associated with intracranial infections such as meningi-tis and meningo-encephalitis. The cause of the cranial nerve palsy was referred to as undetermined if, based on the recorded history, examination and investigations, the specific cause was not apparent.
The Pearson χ2 test was used to determine if there were any statistically significant differences between proportions.
RESULTS
A total of 166 children with paralytic strabismus were identified over the 15-year study period. Age at presen-tation ranged from 1 month to 12 years, with a mean age of 4.2 (± 3.0) years. The majority of patients (64%) were aged less than 5 years. There were 90 boys (54%) and 76 girls (46%), and 123 (74%) of the children were of mixed race ethnicity, while 43 (26%) were black. Twenty-eight (17%) had associated neurological deficits. With regards to time of onset, 91 (55%) patients had congenital para-lytic strabismus, while 75 (45%) cases were acquired.
In this series, 87 children (52%) had fourth cranial nerve palsy, 64 (39%) had sixth nerve palsy, while 9 (5%) patients had third nerve palsy and 6 (4%) had multiple cranial nerve palsies. Fourth nerve palsies were more common (P = 0.02) in mixed race children (71/123, 58%) than in black children (16/43, 37%) whereas sixth nerve palsies were more common (P = 0.019) in black children (23/43, 54%) than in mixed raced children (41/123, 33%). Figure 1 shows the relative frequency of the types of cranial nerve palsies in our mixed race and black children compared with the proportions in Harley’s report.1 The causes of paralytic strabismus in our patients are presented in Table 1.
Fourth Nerve Palsy
The mean age of the 87 patients with fourth nerve palsy was 3.8 (± 2.7) years, with a range of 7 months to 11 years. The majority (61%) were boys, 82% were mixed race, and 6 (7%) had associated neurological deficits. Most cases (75%) were congenital, 13% were of unde-termined origin, 10% were caused by trauma and 2% were due to hydrocephalus. A total of 56 (64%) patients had strabismus surgery.
Sixth Nerve Palsy
The mean age of the 64 patients with sixth nerve palsy was 4.4 (± 3.3) years, with a range of 1 month to 12
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398 B. Olusanya et al.
Ophthalmic Epidemiology
years. The majority (60%) were girls, and 64% were mixed race, while 19 (30%) had associated neurological deficits. Trauma and congenital cases each accounted for 26% (Table 2). None of our patients had recurrent sixth nerve palsies and 18 (28%) went on to have surgery. All three patients with sixth nerve palsies secondary to neoplasia had neurological symptoms at presentation. These included ataxia and headaches in two patients (1 cerebellar astrocytoma, 1 medulloblastoma), the third had a hemiparesis and hemi-facial weakness due to a pontine glioma. None of the patients had an isolated sixth nerve palsy secondary to neoplasm in our series.
Third Nerve Palsy
The mean age of the 9 patients with third nerve palsy was 4.5 (± 3.3) years, with a range of 4 months to 8 years. Two-thirds were boys, and 5 (56%) were mixed race. Two had associated neurological deficits, seven cases were congenital, one was traumatic (following a gunshot injury to the head), and one was undetermined. A total of 6 (67%) patients had strabismus surgery.
Multiple Cranial Nerve Palsies
Five of the 6 patients with multiple cranial nerve palsies had combined fourth and sixth nerve palsies, while one
had third nerve palsy combined with sixth nerve palsy. Their mean age was 6.0 (± 3.8) years with a range of 8 months to 12 years. Five (83%) were boys, and all were mixed race. One had associated neurological deficit. With respect to etiology, two cases were congenital, two were traumatic, one was secondary to Miller-Fisher syn-drome and one was undetermined. Three (50%) were treated surgically.
DISCUSSION
The age and gender distribution of our patients shows a preponderance of children younger than 5 years, with more males than females. This is similar to findings of previous reports.2,4
The racial distribution of our patients, when compared to that of the general population of the Western Cape, indicates an over-representation of mixed race children. Based on the 2001 census, the ratio of mixed race chil-dren to black children was 62.5:37.5, but in our study 74% were mixed race. It appears that the low proportion of black children might be a reflection of unequal access to health care: Black South Africans have been reported to have poorer access.14 There is evidence, however, to suggest that socioeconomic status, rather than race, is the most significant determinant of actual access.15 In addition, black and mixed race South Africans have been shown to have similar access to care when last ill, and both ethnic groups are disadvantaged with regards to health care when compared to white South Africans.15,16
Therefore, we believe that the lower proportion of black children in this series may not be completely explained by inequitable access and referral bias, as the effect of race on access to health care appears to be complex and is confounded by other variables. A population-based study would be required to further elucidate this.
The relative frequencies of the different types of cra-nial nerve palsies in this study differ from a previous hospital-based study of childhood ocular motor nerve
FIGURE 1 Relative frequency of pediatric cranial nerve palsies in South African black and mixed race children compared with a previ-ous study by Harley.1
TABLE 1 Causes of paralytic strabismus in 166 South African black and mixed race children.Etiology n %Congenital 91 55Trauma 29 18Undetermined 27 16Infection 7 4Hydrocephalus 7 4Neoplasm 3 2Others* 2 1Total 166 100*Miller-Fisher syndrome (1), benign intracranial hypertension (1).
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Paralytic Strabismus in South African Children 399
palsies, conducted by Harley.1 Fourth nerve palsy was the most common in our patients; however, it was less common than sixth and third nerve palsies in Harley’s report.1 On the other hand, our finding is similar to the population-based study by Holmes2 (n = 36), in which fourth nerve palsy was most prevalent. Among our black children, sixth nerve palsy was the most common and this finding is more in keeping with Harley’s obser-vation.1 The reason for the difference between black and mixed race children with regards to the nerve most commonly affected in paralytic strabismus is unclear, and requires further investigation.
The etiologies of paralytic strabismus in this study are similar to those reported by Harley and Holmes.1,2 Congenital nerve palsies were foremost, followed by trauma. There was, however, a higher relative propor-tion of children with congenital paralytic strabismus in our series (55%) compared with Harley’s (30%) and Holmes’ (44%)). Neoplasia accounted for a lower percentage in our patients (2%), when compared to Harley’s (17%) and Holmes’s (8%) studies.1,2 Again, the reason for these differences is uncertain and further research in this area is necessary.
In children with acquired paralytic strabismus, trauma was the most common cause in our series (39%). This finding is similar to the 43% reported by Kodsi and Younge.4
Among patients with fourth nerve palsy, the pre-dominance of congenital cases observed in our study is similar to findings of previous reports.1,2,17,18 In pediatric patients, most cases of fourth nerve palsy are either con-genital or due to trauma, while other causes are rare.2 In Kodsi and Younge’s study of acquired fourth nerve palsies, trauma was the most common (37%) followed by undetermined cases (21%).4 We found undetermined cases (13%) to be more common than trauma (10%) in children with acquired fourth nerve palsies.
The main differences in specific etiologies of sixth nerve palsies are shown in Table 2. There was a higher proportion with congenital and undetermined causes in our series, and relatively few neoplasms, compared to other studies.1,5,7,9 These differences may be related to the possibility of bias in the types of patients referred to different tertiary hospitals based on available expertise or reputation of such centers.
When looking at specific causes of acquired sixth nerve palsies, our findings concur with Kodsi and Younge, who found trauma to be the most common.4 However in another study of 133 children with acquired sixth nerve palsies, a large proportion (39%) was due to neoplasms.12
Recurrent sixth nerve palsies are reported to be rare in children, and this is borne out in our series.19,20
Most previous reports have observed more males than females with sixth nerve palsies, with the excep-tion of some studies on benign sixth nerve palsy.5,7,9,19,21 The fact that we found more females in our series is noteworthy.
Causes of third nerve palsy in our children are akin to previous reports, in which congenital cases are most common.1,2,6,10,22 Likewise, trauma was a main cause of multiple nerve palsies in our study as well as previous studies.1,2,4
Limitations of this study largely surround its retro-spective, clinic-based design. The study population is not a true cohort, as only children from the two main ethnic groups were included. Incidence rates of para-lytic strabismus cannot be inferred because the study is not population-based. It is possible that a proportion of children with paralytic strabismus within the popula-tion served by the Red Cross Hospital did not present to our clinic and were therefore not included.
Unavoidable inaccuracies arose in history-taking due to language barriers, and we relied on caregivers’ recollections of the onset of deviation, without the aid of photographs. Nevertheless, this study is the first to provide robust data on the profile of pediatric paralytic strabismus in two large South African ethnic groups.
In this clinic-based study, paralytic strabismus was more common in mixed race children. Fourth nerve palsies predominated in mixed race children, whereas the majority of black children had sixth nerve palsies. As a whole, congenital palsies were the most common etiology, while neoplasia was uncommon. Further pop-ulation-based studies on the epidemiology of paralytic strabismus in children are needed to clarify the role of race as a potential risk factor.
Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the article.
TABLE 2 Causes of pediatric sixth nerve palsy in the present study and in the literature.
EtiologySouth African children Harley1 Lee5 Afifi7 Merino9
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